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Choroidal Findings in Eyes with Birdshot Chorioretinitis Using Enhanced-Depth Optical Coherence Tomography

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Choroidal Findings in Eyes with Birdshot Chorioretinitis Using Enhanced-Depth Optical Coherence Tomography Special Issue Choroidal Findings in Eyes With Birdshot Chorioretinitis Using Enhanced-Depth Optical Coherence Tomography Christian B¨oni,*,1 Jennifer E. Thorne,2 Richard F. Spaide,3 Trucian A. Ostheimer,2 David Sarraf,1 Ralph D. Levinson,1 Debra A. Goldstein,4 Lana M. Rifkin,†,4 Albert T. Vitale,5 Glenn J. Jaffe,6 and Gary N. Holland1 1Ocular Inflammatory Disease Center, UCLA Stein Eye Institute and Department of Ophthalmology, David Geffen School of Medicine at UCLA, Los Angeles, California, United States 2Wilmer Eye Institute and Department of Ophthalmology, Johns Hopkins School of Medicine, Baltimore, Maryland, United States 3Vitreous, Retina, Macula Consultants of New York, New York City, New York, United States 4Department of Ophthalmology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, United States 5Moran Eye Center and Department of Ophthalmology, University of Utah School of Medicine, Salt Lake City, Utah, United States 6Department of Ophthalmology, Duke University, Durham, North Carolina, United States Correspondence: Gary N. Holland, PURPOSE. The purposes of this study were to describe choroidal findings observed using UCLA Stein Eye Institute, 100 Stein optical coherence tomography with enhanced depth imaging (EDI-OCT) in eyes with birdshot Plaza, Los Angeles, CA 90095-7000, chorioretinitis (BSCR) and to test the hypothesis that these findings are related to participant USA; demographics, clinical characteristics, and treatment. [email protected]. METHODS. In a multicenter, cross-sectional study, 172 eyes of 86 individuals with BSCR Current affiliation: *Department of Ophthalmology, University of Zurich, underwent a standardized clinical evaluation, including defined protocols for EDI-OCT Zurich, Switzerland; imaging, with macular and peripapillary volume scans. Choroidal findings were compared to †Ophthalmic Consultants of Boston, demographic information, ophthalmic examination findings, and treatment history, using Massachusetts, and Department of logistic regression models. EDI-OCT images were evaluated by two independent, masked Ophthalmology, Tufts University graders. School of Medicine, Boston, Massa- chusetts, United States. RESULTS. Median age was 56 years old; 54 participants (62.8%) were female. One or more choroidal lesions (a predefined hyporeflective zone) were identified in 105 eyes (63.6%). Submitted: December 9, 2015 Median choroidal thickness was 293 lm. Choroidal lesions were associated with longer Accepted: July 3, 2016 disease durations (odds ratio [OR]: 1.08; P ¼ 0.03), increased vitreous haze (>0.5þ; OR: 4.43; Citation: B¨oni C, Thorne JE, Spaide RF, P ¼ 0.02), presence of macular edema (OR: 3.00; P ¼ 0.02), and thick choroids (OR: 3.89; P et al. Choroidal findings in eyes with ¼ 0.001). Use of immunomodulatory therapy was associated with lower risk of thin choroids birdshot chorioretinitis using en- (lower 25th percentile, OR: 0.17; P ¼ 0.001) or thick choroids (upper 25th percentile, OR: hanced-depth optical coherence to- 0.22; P ¼ 0.002). At least some choroidal lesions did not have corresponding, clinically mography. Invest Ophthalmol Vis Sci. 2016;57:OCT591–OCT599. apparent ‘‘birdshot lesions’’ on fundus examination. DOI:10.1167/iovs.15-18832 CONCLUSIONS. Choroidal abnormalities identified by EDI-OCT imaging are common in the macular and peripapillary regions of eyes with BSCR. Choroidal lesions were associated with clinical signs of inflammation, suggesting that they represent foci of disease activity. EDI-OCT may provide useful information about disease mechanisms and response to treatment in future, longitudinal studies of BSCR. Keywords: birdshot chorioretinitis, EDI-OCT, uveitis ubretinal, hypopigmented spots are an important feature of lesions, or from blockage by the lesions themselves. Monitoring S birdshot chorioretinitis (BSCR), suggesting involvement of the choroid with ICG angiography can be challenging. For the choroid in disease processes.1 In the past, the condition these reasons, alternative techniques for evaluation of anatomic was called ‘‘vitiliginous chorioretinitis,’’ on the assumption that changes in the choroid of eyes with BSCR may be valuable. the choroid became depigmented in isolated regions.2 Subse- Spectral domain optical coherence tomography with en- quent studies have led to the general assumption that these hanced depth imaging (EDI-OCT) may be one such technique. ‘‘birdshot lesions’’ are inflammatory in nature and that they are Using EDI-OCT, Mrejen and Spaide9 demonstrated hyporeflec- similar to fundus changes caused by sarcoidosis,3 and limited tive zones in the choroid of eyes with BSCR. Keane et al.10 histopathologic specimens show foci of lymphocytic infiltra- subsequently reported choroidal depigmentation and hyper- tion.4,5 Birdshot lesions may not represent the full spectrum of reflective foci in the choroid and speculated that these findings disease features, however. For example, indocyanine green were most likely inflammatory in nature. Other choroidal (ICG) angiography may reveal a greater number of hypolucent findings by EDI-OCT included thinning of the Sattler layer, dark spots than the number of birdshot lesions seen generalized choroidal thinning, focal depigmentation, and clinically6À8; these spots could result from choroidal hypoper- presence of a suprachoroidal space.10,11 The clinical relevance fusion, from displacement of vessels by a space-occupying of these findings remains poorly understood. To expand our iovs.arvojournals.org j ISSN: 1552-5783 OCT591 This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License. Birdshot Chorioretinitis and Enhanced-Depth OCT IOVS j Special Issue j Vol. 57 j No. 9 j OCT592 understanding of these choroidal findings, we performed a large, prospective, cross-sectional, multicenter study of people with BSCR, using EDI-OCT. We sought to provide a detailed description of choroidal findings and to identify associations between choroidal findings and other features of the disease. METHODS Study Population We recruited patients with BSCR from University of California Los Angeles, Johns Hopkins University, Northwestern Univer- sity, University of Utah, and Duke University. All study participants met criteria for the diagnosis of BSCR, established by an international group of investigators.12 Individuals with high myopia or hyperopia (spherical equivalent more than 6 diopters [D]), age-related macular degeneration, or diabetic retinopathy were excluded, as these ocular conditions have been associated with choroidal abnormalities on EDI-OCT.13À15 Individuals with media opacities that precluded imaging were also excluded. The study was approved by the institutional review boards at each clinical site, and written informed consent was obtained from each study participant. The study adhered to the tenets of the Declaration of Helsinki for research involving human subjects. FIGURE 1. The OCT imaging protocol included volume scans of the All study participants underwent a standardized set of macular region (centered on the fovea, top row) and the peripapillary imaging studies, visual function tests, and clinical examinations region (centered on the optic disc, bottom row). As shown to the left on a single day, as described below. of each OCT scan, the near-infrared image illustrates the size of the volume scans according to the predefined protocol. Corresponding fundus images were also obtained (not shown). Clinical Evaluations Data collected from each participant included demographic Meditec, Dublin, CA, USA). Humphrey visual field mean information (age, sex); medical history; ophthalmic history deviation (HVF-MD) scores were used in analyses; values of (duration of visual symptoms attributable to BSCR, interval À3.0 decibels (dB) or less were considered abnormal.22,23 since diagnosis of BSCR, surgeries [glaucoma, vitreoretinal], or Ophthalmologic examinations included IOP determination complications of BSCR, including optic disc edema, cystoid by applanation tonometry; assessment of anterior chamber macular edema [CME], choroidal neovascularization, or retinal cells by slit-lamp biomicroscopy (categorized according to SUN vasculitis); and any past or current treatment for BSCR (topical, Working Group recommendations24); quantification of vitreous regional, or systemic medications, such as oral and intravenous inflammatory reactions (as described by Nussenblatt and corticosteroids, dexamethasone implant [Ozurdez; Allergan, associates25); dilated indirect ophthalmoscopy (noting the Inc., Irvine, CA, USA], fluocinolone acetonide implant [Re- presence or absence of optic nerve abnormalities; CME, tisert; Bausch and Lomb, Rochester, NY, USA], immunomodu- choroidal neovascularization, or retinal vasculitis). For study latory agents [methotrexate, mycophenolate mofetil, azathioprine, cyclosporine, tacrolimus, infliximab, adalimu- purposes, active disease was defined as a vitreous haze score of mab], glaucoma medications, or anti-VEGF agents). ‡0.5þ. Presence of CME was confirmed with OCT. A questionnaire was administered at the study visit to determine the presence or absence of eight prospectively Image Acquisition Protocol and Image Analysis defined visual symptoms in each eye (blurry vision, floaters, The Spectralis HRA OCT (Heidelberg Engineering, Heidelberg, nyctalopia, abnormal contrast sensitivity, abnormal color þ vision, vibrating vision, metamorphopsia, and decreased Germany) was used at each site to acquire macular and peripheral vision).16 Four measurements
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